Abstract
The migration of border cells during Drosophila melanogaster oogenesis is a simple and powerful system for studying invasive cell migration in vivo. Border cells are somatic cells that delaminate from the follicular epithelium of an egg chamber and invade the germ line cluster. They migrate between the nurse cells to reach the oocyte1,2, using DE-cadherin for adhesion to the substratum3. Border cells take approximately 6 h to migrate a distance of 100 μm4. The migration is guided by EGFR (epidermal growth factor receptor) and PVR (platelet-derived growth factor (PDGF)/vascular endothelial growth factor (VEGF) receptor)5,6. Here, we show that a single long cellular extension (LCE), several cell diameters in length, is formed at the initiation of migration. The LCE may function as a 'pathfinder' in response to guidance cues. LCE growth requires directional guidance signals and specific adhesion to the substratum. Interference with actin–myosin interactions allows continued LCE growth while preventing translocation of the cell bodies. We discuss similarities between LCEs and axons and the use of LCE-like structures as a general mechanism for initiating invasive migration in vivo.
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References
King, R. C. Ovarian Development in Drosophila melanogaster (Academic Press, New York, 1970).
Montell, D. J., Rørth, P. & Spradling, A. C. Cell 71, 51–62 (1992).
Niewiadomska, P., Godt, D. & Tepass, U. J. Cell Biol. 144, 533–547 (1999).
Spradling, A. in The Development of Drosophila melanogaster 1–70 (Cold Spring Harbor Laboratory Press, NY, 1993).
Duchek, P., Somogyi, K., Jékely, G., Beccari, S. & Rørth, P. Cell 107, 17–26 (2001).
Duchek, P. & Rørth, P. Science 291, 131–133 (2001).
Verkhusha, V. V., Tsukita, S. & Oda, H. FEBS Lett. 445, 395–401 (1999).
Loureiro, J. J. et al. Dev. Biol. 235, 33–44 (2001).
Parent, C. A. & Devreotes, P. N. Science 284, 765–770 (1999).
Firtel, R. A. & Chung, C. Y. BioEssays 22, 603–615 (2000).
Funamoto, S., Meili, R., Lee, S., Parry, L. & Firtel, R. A. Cell 109, 611–623 (2002).
Iijima, M. & Devreotes, P. Cell 109, 599–610 (2002).
Westphal, M. et al. Curr. Biol. 7, 176–183 (1997).
Aizawa, H., Sameshima, M. & Yahara, I. Cell Struct. Funct. 22, 335–345 (1997).
Edwards, K. A. & Kiehart, D. P. Development 122, 1499–1511 (1996).
Rørth, P., Szabo, K. & Texido, G. Mol. Cell 6, 23–30 (2000).
Knight, B. et al. Curr. Biol. 10, 576–585 (2000).
Kulesa, P., Bronner-Fraser, M. & Fraser, S. Development 127, 2843–2852 (2000).
Koster, R. W. & Fraser, S. E. Curr. Biol. 11, 1858–1863 (2001).
Yee, K. T., Simon, H. H., Tessier-Lavigne, M. & O'Leary, D. M. Neuron 24, 607–22. (1999).
Rørth, P. et al. Development 125, 1049–1057 (1998).
Wimmer, E. A., Cohen, S. M., Jackle, H. & Desplan, C. Development 124, 1509–1517 (1997).
Bunch, T. A., Grinblat, Y. & Goldstein, L. S. B. Nucleic Acids Res. 16, 1043–1061 (1988).
Lee, T. & Luo, L. Neuron 22, 451–461 (1999).
O'Keefe, L. et al. Development 124, 4837–4845 (1997).
Leevers, S. J., Weinkove, D., MacDougall, L. K., Hafen, E. & Waterfield, M. D. EMBO J. 15, 6584–6594 (1996).
Oda, H., Uemura, T., Harada, Y., Iwai, Y. & Takeichi, M. Dev. Biol. 165, 716–726 (1994).
Clark, I. E., Jan, L. Y. & Jan, Y. N. Development 124, 461–470 (1997).
Britton, J. S., Lockwood, W. K., Li, L., Cohen, S. M. & Edgar, B. A. Dev. Cell 2, 239–249 (2002).
Acknowledgements
We are grateful to C. Wilson, A. González-Reyes, Y.N. Jan, S. Leevers, W. Lockwood and the Bloomington stock center for flies, to A.-M. Voie for embryo injections and to S. Cohen for comments on the manuscript. T.A.F. was supported by a pre-doctoral fellowship from Louis-Jeantet foundation.
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Figure S1. PI3K and PTEN do not affect LCEs and border cell migration. (PDF 462 kb)
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Fulga, T., Rørth, P. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat Cell Biol 4, 715–719 (2002). https://doi.org/10.1038/ncb848
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DOI: https://doi.org/10.1038/ncb848
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